( Curcuma Longa) Rhizome Extracts on Aphids Control, Plant Growth And

Journal of Applied Botany and Food Quality 91, 194 - 201 (2018), DOI:10.5073/JABFQ.2018.091.026

1Department of Botany, Kohat University of Science and Technology (KUST), Kohat, Pakistan 2National Institute for Food and Agriculture (NIFA) Peshawar, Pakistan 3Department of Microbiology, Abdul Wali Khan University Mardan, Pakistan 4Department of Biotechnology and Genetic Engineering, Kohat University of Science and Technology (KUST), Kohat, Pakistan 5Department of Botany, Abdul Wali Khan University Mardan, Pakistan Effects of Neem (Azadirachta indica) seed and Turmeric (Curcuma longa) rhizome extracts on aphids control, plant growth and yield in okra Uzair Muhammad1, Tariq Nawaz Khattak2, Hazir Rahman3, M.K. Daud4, Waheed Murad5, Azizullah Azizullah1* (Submitted: June 3, 2017; Accepted: March 12, 2018)

Summary proximately 1.1 billion pounds of pesticides were used during 2006- 07, which was 22% of the total pesticides used worldwide (Kiely The use of synthetic pesticides to control pests and increase crop et al., 2004). Only to some extent, pesticide use has enabled farmers yield is a common practice, but they cause several environmental and to minimize crop losses caused by pest attacks (Hamill et al., 2004). health problems. Therefore, there is a need to explore alternative ap- Despite their useful effect of protecting crops, synthetic pesticides proaches to reduce the sole dependence on synthetic pesticides. The cause hazardous impacts on the surrounding environment by affec- present study was conducted to screen the extracts of Neem seed ting non-target organisms. The use of pesticides kill targeted orga- and Turmeric rhizome for pesticidal activities against okra pests nism but as well as kill some beneficial organisms alsoG ( ilden (aphids: Aphis gossypii). Experiments were conducted in field with et al., 2010). Synthetic pesticides have serious effects on human four plots. One plot was kept as a control (unsprayed) and one was health and cause various disorders like breast cancer, the suppres- sprayed with synthetic pesticides, one with Neem seeds extract and sion of immune system, disorder of nervous system, respiratory dis- one with Turmeric rhizome extract. The effect on number of pests, order and hormonal damages (Benbrook, 2004). Some chemicals plant growth and yield was observed at regular intervals. A signifi- of the commercial pesticides have been investigated for the disrup- cant reduction in pests was recorded in all treatments as compared tion of male reproductive hormones, low sperm count in men and to the control. Neem seed extract was more effective than Turmeric birth defects in babies (Deepa et al., 2011). It has been estimated rhizome extract as revealed by 73% decrease in aphids by Neem ex- that about $1.1 billion dollar per year are spent worldwide on public tract in comparison to 54% by Turmeric extract after last application. health problems associated with pesticide-related acute poisonings Both the extracts were found to be more effective than the synthetic and cancer (Benbrook, 2004). In addition to their adverse effects pesticides in controlling okra pests. Both the extracts had stimulatory on animals and humans, pesticides also adversely affect non-target effects on okra growth and yield. For example, the total yield of plots plants. They reduce metabolite synthesis and translocation and in- sprayed with Neem (53.3 kg plot-1) and Turmeric extract (47.7 kg hibit the processes like photosynthesis, respiration and sterol syn- plot-1) was higher than the yield of control plot (33.8 kg plot-1) and thesis in non-targeted crops like tomato, maize, pea, grapes, bean plot sprayed with synthetic pesticides (39 kg plot-1). It is concluded and barley (Magné et al., 2006). Pesticides have some direct harmful that Neem and Turmeric extracts can be used as alternative of syn- effect on non-target plant growth such as shoot yellowing, poor root thetic pesticides for controlling pests’ attacks in okra. hair development and reduced plant growth (Walley et al., 2006). Pesticides also affect size, number and morphology of fruits and Key words: Neem, Turmeric, Aphids, Okra, pesticidal properties, seeds which can lead to reduce yield and low quality (Magné et al., growth and yield 2006). In comparison, plants derived pesticides or botanical extracts are non-toxic to the user, easily biodegradable and specific in their action and can serve as models for the development of new synthetic Introduction analogues with favorable biological and physicochemical properties Food crops are generally attacked by a number of pests like insects, (Akbar et al., 2010). weeds, and other pathogens which cause substantial losses in agricul- Neem (Azadirachta indica) is a large tree with semi-straight to ture. Crop losses due to different factors like diseases, animal pests straight trunk and spreading branches. It has been widely regarded and weeds range between 20 and 40% of the total yield (Savary as a natural source of pesticides and other agrochemicals. Neem was et al., 2006). According to some estimations, the total loss (without reported to be the most effective among the 2,400 plant species that crop protection practices) due to pests varied from about 50% in have shown pesticidal activities (Girish and Shankara, 2008). The wheat to more than 80% in cotton (Dhaliwal et al., 2002). Generally, extracts of different parts of Neem (leaves, seeds and bark) were crops are attacked by more than 10,000 species of insects, 30,000 found to control a variety of arthropods, nematodes, fungi, viruses, species of weeds and by a thousand species of nematodes (Dhaliwal snails and crustacean species (Girish and Shankara, 2008). The ex- et al., 2010). In addition, about 100,000 diseases in plants are caused tract of its seeds was effective larvicidal and indicated 70-90% mor- by fungi and other microorganisms (Dhaliwal et al., 2010). tality against Culex larvae (Hashmat et al., 2012). Neem extract was It has been observed during the last 40 years that despite a continu- recommended as the most promising pesticide for effective control of ous increase in pesticide application, pest attacks have not been sig- tomato fruit worm, Helicoverpa armigera (Shah et al., 2013). nificantly controlled and crops losses continue (Pimentel, 2007). Turmeric (Curcuma longa) is the rhizomatous perennial plant of Approximately 5.2 billion pounds of total pesticides were used the family Zingiberaceae (ginger family). It possesses a variety of worldwide during 2006 and 2007, with 40% herbicides, 17% insec- bioactive ingredients that act as repellent and insecticidal agents ticides and 10% fungicides (Kiely et al., 2004). Only in the U.S, ap- (Damalas, 2011). Rhizomes powder of turmeric showed repellency against different insects of stored products like Sitophilus granaries, * Corresponding author Tribolium castaneum, and Rhyzopertha dominica (Damalas, 2011). Effects of Neem seed and Turmeric rhizome extracts on aphids control in okra 195

Its extract was also effective against rice insect Sitophilus oryzae Materials and methods (Damalas, 2011). Turmeric powder with ash showed pesticidal acti- Experimental field vity against different pests of rice (Oxya nitidula and Cnaphalocrocis The present experiments were conducted at Nuclear Institute for medinalis) and eggplant (Epilachna vigintioctopunctata) (Sankari Food and Agriculture (NIFA) Peshawar, Pakistan. Okra was grown in and Narayanasamy, 2007). Similarly, its rhizomes powder was plots with a size of 88 × 17 feet. The experimental field was consisted shown to be effective against store-grain pests like lesser grain borer of four main plots: one each for the control (no treatment), synthetic (Rhyzopertha dominica) in rice (Chander et al., 2003). pesticides (Cypermethrin and Bifenethrin), Turmeric rhizome extract Okra (Abelmoschus esculentus) is one of the hot summer and annual and Neem seeds extract (Fig. 1). Each plot was further divided into vegetable grown in plain areas of the world. In Pakistan, Okra is cul- three equal blocks. Each plot was sprayed with the respective solution tivated on an area of about 2.21 × 105 hectares (Kashif et al., 2008). at specific intervals as shown in Tab. 1. Normal agronomic practices It is attacked by a number of insects which reduces its growth and like soil preparation, irrigation and fertilization were done. yield. Some of the major destructive insect pests of okra are aphids (e.g. Aphis gossypii), whitefly (e.g. Bemisia tabaci), jassid (e.g. Amrasca devastans), thrip (e.g. Thrips tabaci) and spotted bollworm Tab. 1: Dates of extracts application and pests observations. (e.g. Helicoverpa armigera) (Aziz et al., 2012). Among these insects, aphids are the major pests of okra in Pakistan (Gardiner et al., Application of extracts/ Application date Pests observation date 2009). Aphid infestation causes heavy losses in different crops. For pesticides example, aphids attack causes a reduction of up to 4.57% in wheat 1st 15.05.2014 21.05.2014 yield in Pakistan (Khan et al., 2012). Aphids damage maize crops 2nd 26.05.2014 01.06.2014 and cause up to 60% loss in yield (Hafeez and Zia, 2009). Aphids rd also act as a vector and transfer several viruses in potato crops and 3 03.06.2014 11.06.2014 th cause yield losses up to 90% depending on cultivar, infestation and 4 16.06.2014 25.06.2014 th environmental conditions (Saljoqi, 2009). According to an estimate, 5 30.06.2014 06.07.2014 Aphis gossypii causes about 20-40% yield losses in cotton crops in 6th 10.07.2014 18.07.2014 Pakistan (Aslam et al., 2004). Keeping in view the economic importance of okra and losses in its yield due to pest attacks, the present study was conducted to evaluate the extract of Neem seeds and Preparation of plant extracts and pesticides solution Turmeric rhizome for pesticidal activities against aphids in okra to Neem seeds and Turmeric rhizome were purchased from Qissakh- provide an easy and cost effective way for the control of aphid attack wani Bazar in Peshawar. Dried seeds of Neem and rhizome of on okra in Pakistan. Turmeric were crushed with electronic blender separately. The ob-

Fig. 1: Images of experimental plots. (a) Control plot, (b) pesticides treatment plot (c) Turmeric treatment plot, (d) Neem treatment plot. 196 U. Muhammad, T.N. Khattak, H. Rahman, M.K. Daud, W. Murad, A. Azizullah tained powder was mixed with petroleum ether at the rate of 125 g Determination of fruit length per liter following the method of Soxlet. The mixture was stirred by Three fruits per plant were collected from 20 plants in each block of orbital shaker for five days and then was filtered through fine gauze every plot and the fruit length was determined in cm using a measu- to remove bigger pieces. The extract was then mixed with 5 liters of ring tape. water to prepare the final solution for application A( ziz et al., 2012). Average fruit length (cm) = Sum of total length of fruits / total num- For comparison purpose, two synthetic pesticides, i.e. Cypermethrin ber of fruits and Bifenethrin, were applied in a mixture form by dissolving 10 ml of each pesticide in 5 liters of water. Determination of okra yield For measuring the okra yield, the fruits were plucked after every four to five days and the yield was measured by an electronic balance in Application/spray of extracts kilogram (kg). The prepared extracts and synthetic pesticides solutions were applied on their respective plots at different time intervals as shown in Tab. 1, while the control plot was left unsprayed. The first spray was applied Data analysis after the appearance of pests. All solutions were applied on the same Mean and standard deviation of the three replicates for each param- day using a knapsack sprayer. The sprayer was rinsed with clean wa- eter were calculated using Microsoft Excel. One-way analysis of ter before using for each solution. A total of six applications were variance (ANOVA) was applied to measure the significance of dif- made for each treatment at different times as shown in Tab. 1. ferences among different treatments and the control. The difference was considered to be significant if p value was smaller than 0.05 (p < 0.05). Pest monitoring For the investigation of extracts effect on pests, the number of pests per plant and percentage of infected plants were determined after Results each application. A total of 20 plants were randomly selected in each Effect of Neem and Turmeric extracts on aphids block of every plot. To collect aphids, a piece of paper was laid under Effect on percentage of infected plants one side of plant, shaken the plant gently on the paper and collected The percentages of infected plants in different plots are shown in the aphids. The average number of aphids per plant was calculated Tab. 2. All the applied solutions, i.e., the Neem and Turmeric ex- and the percentage of infected plants in each block was determined. tracts and the synthetic pesticides significantly protected okra plants A total of six observations were made at specific interval during the from aphid attacks. In the first observation (after first application), course of experiment as shown in Tab. 1. there were 53.33%, 81.66% and 70% infected plants in Neem extract, Turmeric extract and pesticides treated plots, respectively, as compared to 90% in the control. In the second observation (after Determination of plant growth and yield parameters second application) 50%, 78.33% and 70% plants were attacked by Determination of shoot length aphids in Neem, Turmeric and pesticides treated plots, respectively, After sixty days of plant growth, three plants were randomly collec- as compared to 85% in the control. The reduction in aphids attacks by ted from each block of every plot. The shoot length in centimeter Turmeric extract was statistically not significant as compared to the (cm) was measured with a measuring tape. The average shoot length control, but the Neem extract caused a significant reduction in aphids was calculated as follow: attacks as compared to the control and pesticides. After third spray, Average shoot length (cm) = Sum of length of all plants/ total number 45%, 60% and 63.33% plants were infected by aphids in Neem, of plants Turmeric and pesticides treated plots, respectively, where 80% plants in the control were attacked. In this case both Neem and Turmeric extracts significantly controlled aphids attacks in comparison to the Determination of leaf area control, but the difference was statistically significant only in the case Three leaves per plant were collected from randomly selected 20 of Neem extract when compared to the plot sprayed with synthetic plants in each block of every plot. The leaf area (cm2) was calculated pesticides. Both the extracts were shown to be more effective with the from the length and width of a leaf. passage of time as revealed from third spray and observation onward, where both the Neem and Turmeric extracts caused a more prominent and significant reduction in aphids attacks as compared to the control. Determination of fruits number Although a natural decrease in pest attacks was observed with time For the determination of fruit number, three plants were randomly as revealed by the number of infected plants in the control plot at dif- selected in each block of every plot and the number of fruits per plant ferent observation, a prominent effect of Neem and Turmeric extracts was calculated as: can be observed in comparison to the control. The extracts, especially Average number of fruits per plant = Sum of total number of fruits / Neem extract was found to be more effective even than the synthetic total number of plants pesticides (Tab. 2).

Tab. 2: Percentage of infected okra plants observed at six different intervals.

1st 2nd 3rd 4th 5th 6th Control plot 90±00a 85±05a 80±00a 68.33±2.88a 60±00a 60±00a Pesticides plot 70±00b 70±00b 63.33±2.88b 63.33±2.88b 36.66±5.77b 36.66±5.77b Turmeric plot 81.66±5.77a 78.33±7.63a 60±00b 46.66±5.77b 33.33±5.77b 33.33±5.77b Neem plot 53.33±2.88c 50±00c 45±00c 33.33±7.63b 23.33±5.77c 23.33±5.77c

Values given are mean ± standard deviations of three replicates. Different letters on each two values indicate significant difference from each other. Effects of Neem seed and Turmeric rhizome extracts on aphids control in okra 197

Effects on number of Aphids per plant The effect of Neem and Turmeric extracts on number of aphids per plant is shown in Fig. 2. The obtained results indicate that after first two applications, no treatment caused any significant decrease in Aphids density per plant in comparison to the control. However, thereafter both the Neem and Turmeric extracts were shown to cause a decrease in the number of Aphids per plant in comparison to the control as well as pesticides treated plot. For example, after third observation, there were 18.66 and 20.66 (mean values) of aphids per plant in Neem and Turmeric treated plots, as compared to 25.66 and 27.66 in the control and pesticides treated plot, respectively. The same trend continued and both the extracts were observed to decrease the number of aphids per plant in all the remaining observations. Both the extracts were found to show enhanced protection with the passage of time and repeated application. For example, after sixth and last application, there were only 5.66 and 9.66 (mean) aphids per plant in Fig. 3: Shoot length of okra in four experimental plots measured after three Neem and Turmeric treated plots in comparison to 17 and 21 aphids months of growth. The chart bars show the mean value of three repli- in pesticides and control plots, respectively. After last application, cates in each set of experiment while the standard deviation is shown Neem and Turmeric caused a 73 and 54% reduction in the number by error bars (Cont. means control plot). of aphids per plant, respectively. It was also observed that both the extracts were more effective than the synthetic pesticides as revealed by the obtained results (Fig. 2). Although after fourth application, the synthetic pesticides significantly controlled aphids in comparison to the control plot but this effect was much smaller than the Neem and Turmeric extracts. A comparison of both the extracts revealed that Neem seeds extract was more effective than the Turmeric rhizome extract as can be seen by a 73% decrease in aphids by Neem extract in comparison to 54% by Turmeric extract after last application. It is noteworthy to mention that like the natural decrease in the percentage of attacked plants, a natural decrease in the number of aphids per plant was observed as is evident from the data of control plot at different intervals (Fig. 2).

Fig. 4: Area of okra leaf in the four experimental plots measured after three months of growth. The chart bars show the mean value of three replicates in each set of experiment while the standard deviation is shown by error bars. Different letters on different chart bars indicate significant difference from each other (Cont. means control plot).

ticides treated and control plots, respectively. Both the extracts were shown to cause a slight but statistically significant increase in the leaf area of okra (Fig. 4), and the average leaf area in in plants sprayed with Neem and Turmeric extracts reached 193.26 and 192.66 cm2 in comparison to 187.66 and 183.9 cm2 in pesticides treated and control plots, respectively.

Effect on yield parameters Effect on fruit yield Fig. 2: Number of aphids per okra plant noted at different observations. The chart bars show the mean value of three replicates in each set The effect of Neem and Turmeric extracts on fruit yield in term of of experiment while the standard deviation is shown by error bars. weight is shown in Fig. 5. All the applied solutions (Neem, Turmeric Different letters on different chart bars indicate significant difference extracts and synthetic pesticides) significantly protected the okra from each other. plants from aphid attacks and resulted in high yield. In first two plucking periods, there was no increase in fruit yield in Neem, Turmeric and pesticides treated plots in comparison to the control. Effects of plant extracts on growth parameters of okra However, thereafter both Neem and Turmeric extracts increased its In order to evaluate whether the application of Neem and Turmeric yield in comparison to the control as well as pesticides treated plots. extracts for pest control will have any adverse effect on plant growth, For example, in third plucking period there were 8.6 kg, 8.5 kg and the effect of both extracts on two growth parameters (shoot length 8.0 kg fruit yields in Neem, Turmeric and pesticides treated plots, and leaf area) was investigated (Figs. 3 and 4). Both the extracts did respectively, as compared to 7.0 kg in the control. The same trend not cause any adverse effect on shoot length of okra, but rather caused continued and both the extracts were observed to increase fruits yield a slight and non-significant increase in shoot length. Plots sprayed in all the remaining observations. Both the extracts were found to with Neem and Turmeric extracts, the average shoot length was give higher yield with the passage of time and repeated application as 148.83 and 146.10 cm in comparison to143.90 and 142.20 cm in pes- compared to the control. For example, in ninth plucking period there 198 U. Muhammad, T.N. Khattak, H. Rahman, M.K. Daud, W. Murad, A. Azizullah were 5.0 kg and 4.0 kg fruits yield in Neem and Turmeric extracts treated plots as compared to 1.2 kg and 1.8 kg in the control and pesticides treated plots, respectively. In tenth plucking period there were 6.0 kg and 4.5 kg fruits yield in Neem and Turmeric treated plots in comparison to 0.5 kg and 1.2 kg in the control and pesticides treated plots, respectively. It was also shown that both the extracts were more effective than the synthetic pesticides as revealed by the obtained results (Fig. 5). Although after fourth application, synthetic pesticides increased fruits yield in comparison to the control plot but this effect was much smaller than the Neem and Turmeric extracts. A comparison of both the extracts revealed that Neem seeds extract was more effective than the Turmeric rhizome extract as can be seen by 6.0 kg fruits yield by Neem extract in comparison to 4.5 kg by Turmeric extract after last application. The obtained results (Figs. 5 and 6) revealed that a natural decrease in fruits yield was observed with the passage of time as is evident from the data of control plot at different intervals. The effect of Neem and Turmeric extracts on total fruits yields of okra in term of weight is shown in Fig. 6. The mean data indicated Fig. 7: Number of fruits per okra plant in the four experimental plots. that both the Neem and Turmeric extracts caused an increase in total The chart bars show the mean value of three replicates in each set yield (kg) in comparison to the control and synthetic pesticides trea- of experiment while the standard deviation is shown by error bars. ted plots. For example, there were total 53.3 kg and 47.7 kg of fruit Different letters on different chart bars indicate significant difference from each other (Cont. means control plot). in Neem and Turmeric extracts treated plots in comparison to 33.8 kg and 39.0 kg in the control and pesticides treated plots, respectively. Effect on fruit length The average fruit length of okra in different plots is shown in Fig. 8. There was no prominent effect of any extract on fruit length in okra except a slight but significant increase by the Neem extract.

1st 2nd 3rd 4th 5th 6th 7th 8th 9th 10th 11th Yield Yield Yield Yield Yield Yield Yield Yield Yield Yield Yield

Fig. 5: Yield of okra measured at different intervals.

Fig. 8: Average length of fruit in different plots. The chart bars show the mean value of three replicates in each set of experiment while the standard deviation is shown by error bars. Different letters on different bars indicate significant difference from each other (Cont. means control plot).

Discussion Crop losses due to pest attacks is one of the major global problems. Application of chemical pesticides is the most common and success- Fig. 6: Total yield of okra (sum of yield of all observations) in four different ful methods for pests’ control, but synthetic pesticides often have plots. undesirable side effects on the environment such as damaging of non-targeted organisms and accumulation as residue in the environment and food. Therefore, researchers have always been in search Effect on fruit number per plant of pesticides that are more environmentally friendly and safer from The effect of different treatments on fruit number per okra plant is health point of view. This search has led to screening of plants for shown in Fig. 7. The obtained results indicate that the extracts of both their pesticidal activities against common pests which has resulted in plants caused a significant increase in fruit number per plant. The reporting a number of plant species as promising candidates for use average number of fruits on a plant in the control plot was 9.33 which as a source of new plants derived pesticides. reached 19.66 and 16.66 in plots sprayed with Neem and Turmeric The present study was conducted to screen the extracts of Neem extracts, respectively. seeds and Turmeric rhizome against aphids in okra, which causes Effects of Neem seed and Turmeric rhizome extracts on aphids control in okra 199 huge losses of okra every year. It was observed that the extracts of the most effective among Neem, Turmeric and Garlic extracts when both plants effectively reduced plant infestation by aphid as revealed tested against Oxycaremus loetus. by the percentage of infected plants and number of aphids per plant. The pesticidal activities of Neem and Turmeric have been at- The present observations are comparable to previous reports that ex- tributed to the presence of a number of active compounds in them tracts of plants like tobacco and Neem effectively reduced the popu- (Tab. 3). Extracts of these plants might have controlled aphids by lation of bollworm in okra where 11-13% plants were damaged in acting as repellent, antifeedant and/or as growth and reproductive in- treated plot as compared to 25-29% in untreated control (Shabozoi hibitors. A previous report suggested that Neem can act as repellent et al., 2011). Similarly, the extracts of Neem, Turmeric, Garlic and and larvicidal as well as affects egg hatching and reduces fertility Henge significantly reduced jassids population in okra (Sohail et al., in insect pest which results in their progeny inhibition. It can also 2015). Another study reported that the extract of Turmeric caused disturb chemoreceptors of insects and impair their feeding (Iqbal a noticeable reduction (36%) in the population of insect Sitophilus et al., 2006). Turmeric had also been found to possess a variety of oryzae in rice crop (Damalas, 2011). Turmeric rhizomes was found bioactive constituents which acts as a repellent and interfere insect to significantly reduce insects of eggplantEpilachna ( vigintiocto- behavior and growth (Damalas, 2011). According to previous re- punctata) and pests of okra including Amrasca devastans, Anomis ports extracts of plants like Neem, Turmeric, Harmal and Sweet flag flava, Dysdercus cingulatus, Earias vittella, Oxycarenus hyalinipen- showed repellent effect against red flour beetle in wheat (Matter nis, Tetranychus neocaledonicus, and Spodoptera litura (Damalas, et al., 2008). Compounds like Azadirachtin A and B, Salannin and 2011). Furthermore, the extracts of plants in the present study, par- Meliantriol present in Neem have found to protect from insects due ticularly of Neem, were found to be more effective than the synthetic to their repellent effects (James et al., 2014). The passage of time pesticides. This observation is supported by a previous report that and repeated applications of extracts in the present study were found botanical pesticides, like Neem and Tobacco extracts, had similar or to enhance the effectiveness of extracts. It is similar to a previous even higher inhibitory effect against pests as compared to the con- reports where Neem extract was found to cause a higher mortality ventional pesticides (Shabozoi et al., 2011). Another study found of bollworm in okra as exposure time increased (Ahmed, 2000). that Neem extract showed the highest activity against the insect pest, Similarly, Adesina and Afolabi (2014) observed that plant extracts red flour beetle (caused 68.69% reduction) followed by Sweet flag, were less effective after initial applications but killed 89% of flea Harmal and Turmeric extracts (Iqbal et al., 2010). Similarly, Hossain beetles with the passage of time. This enhancement could be due to et al. (2013) reported that Neem extract was more effective than syn- richness of pesticidal activities of neem seed and turmeric rhizome thetic pesticides like carbamate butocarboxin against pests in Tomato, extracts. The insects continued to feed on the treated plants for some Onion and Okra. A comparison of the effectiveness of the extracts of time which caused increase in its efficiency S( chmutterer, 1990). the two plants used in this study revealed that Neem seeds extract In order to evaluate whether the application of Neem and turmeric was more effective than the Turmeric rhizome. It is supported by a extracts for pest control would have any adverse effect on okra previous study of Schmutterer (1990) who found that Neem was growth and yield, the effect on plant growth and fruit yield was ob-

Tab. 3: Some bioactive compounds from Neem seeds and Turmeric rhizomes.

Neem Compounds Biopesticidal activities against aphids References

Azadirachtin A, B Antifeedancy, (Su, 1999; Iqbal et al., 2006; James et al., 2014 Nimbolide Oviposition repellency, reduced in life span, and Lokanadhan et al., 2012) Nimbin mortality, larval growth inhibition, Sodium nimbidate interruption of aphid reproduction, Mahmoodin blocking the development of vector-borne pathogen, Salannin growth regulation, Tetranotriterpenoid (limonoid) fecundity suppression, Salannol sterilization Azadirachtin C, G Salannolacetate Methoxyazadirachtin Vilasinin Nonterpenoidal 2,3-dehydrosalannol Turmeric Compounds Biopesticidal activities against aphids

Curcuminoids Mortality, (Li et al., 2011; Roy et al., 2015; Curcumin I adult repellency, Siddiqi et al., 2011 and Abida et al., 2009) Curcumin II changes in biological fitness, Curcumin III fecundity suppression and sterilization, Sesquiterpenes antifeedant, Turmerone growth-inhibiting effect, Demethoxycurcumin fumigant toxicity, Turmeronol A, B reduced oviposition and eggs hatching Curcumenone Curcumanolide A Tetrahydroxycurcumin Cyclocurcumin Monoterpen Curculonone A, B, C, D 200 U. Muhammad, T.N. Khattak, H. Rahman, M.K. Daud, W. Murad, A. Azizullah served. We found that these extracts had a positive impact on okra Anopheles gambiae. Pharma. Biol. 46, 279-282. growth and yield. Ostermann (1992) also found that in Neem seed Akbar, M.F., Haq, M.A., Parveen, F., Yasmin, N., Khan, M.F., 2010: extract caused an increased growth of okra plants. The higher growth Comparative management of cabbage aphid (Myzus persicae) (Sulzer) and yield by these extracts can be attributed to the low incidence of through Bio and Synthetic-Insecticides. Pakistan Entomol. 32, 12-17. pest attacks as revealed by Hossain et al. (2013). The lower growth Ascher, K.R., 1993: Nonconventional insecticidal effects of pesticides avail- and yield in the control can be probably due to high occurrence of able from the neem tree (Azadirachta indica) Arch. Insect Biochem. aphids. Untreated plants possess high numbers of aphids which have Physiol. 22, 433-449. caused leaf damages, reduced photosynthesis and consequently re- Aslam, M., Razaq, M., Shah, S.A., Ahmad, F., 2004: Comparative effi- duced growth and yield. The reduction in the number of aphids on cacy of different insecticides against sucking pests of cotton. Journal of okra plants sprayed with plant extracts resulted in superior vegetative Research (Science), Bahauddin Zakariya University, Multan, Pakistan growth which in turn produced higher okra fruit yields. Neem extract 15, 53-58. when applied as pesticide was found to give better yield than conven- Aziz, M.A., Hasan, M., Ali, A., Suhail, A., Sahi, T., 2012: Role of different tional pesticides (Satti and Nasr, 2008). Extracts of other plants like physico-chemical characters of okra as a host plant preference of Earias garlic and henge were also found to effectively reduce the population spp. Pak. J. Zoo. 42, 361-369. of pests in okra and increased its yield (Mudathir and Basedow, Benbrook, C., 2004: Why Organic. Int. J. Agric. Sustain. 2, 1. 2004). Similarly, Neem and tobacco extracts increased cotton yield Chander, H., Nagender, A., Ahuja, D.K., Berry, S.K., 2003: Effect of to 1450 kg/ha as compared to the 1000 kg/ha in the control (Rajaram various plant materials on the breeding of lesser grain borer (Rhyzo- et al., 2006). pertha dominica) in milled rice in laboratory. J. Food Sci. and Technol. 40, 482-485. Damalas, C.A., 2011: Potential uses of turmeric (Curcuma longa) products Conclusions as alternative means of pest management in crop production. J. Plant It is concluded that Neem seeds and Turmeric rhizome extracts ef- Omics. 4, 136. fectively controlled aphid’s attacks on okra and enhanced it growth Deepa, T.V., Lakshmi, G., Lakshmi, P.S., Sreekanth, S.K., 2011: Ecological and yield. Both extracts were found to be more effective than the syn- effects of pesticides, Pesticides in the modern world-Pesticides use and thetic pesticides. Based on the present results and previous literature management. Dr. Margarita Stoytcheva (Ed.), ISBN: 978-953-307-459-7, reviewed here, the extracts of Neem seeds and Turmeric rhizome are InTech. recommended as effective, ecofriendly, cheap, and easily available Dhaliwal, G.S., Arora, R., Babu, B.S., Varaprasad, K.S., Anitha, K., remedy for aphids attack in okra. Prasada, Rao, R.D., Chakrabarty, S.K., Chandurkar, P.S., 2002: Estimation of losses due to insect pests in field crops. In resources management in plant protection during twenty first century, Hyderabad, Acknowledgement India, Plant Protection Association of India 1, 11-23. We are thankful to NIFA, Peshawar and KUST, Kohat for supporting Dhaliwal, G.S., Jindal, V., Dhawan, A.K., 2010: Insect pest problems and this study. crop losses: changing trends. Ind. J. Ecol. 37, 1-7. Gardiner, M.M., Landis, D.A., Gratton, C., DiFonzo, C.D., O’neal, M, Chacon, J.M., Wayo, M.T., Schmidt, N.P., Mueller, E.E., Heimpel, Conflict of interest G.E., 2009: Landscape diversity enhances biological control of an in- All authors have participated in this work and all have read and ap- troduced crop pest in the north central USA. Ecological Application. 19, proved the final version of the manuscript. The authors declare no 143-54. conflict of interest. The paper was a part of M.Phil thesis of Mr. Uzair Gilden, R.C., Huffling, K., Sattler, B., 2010: Pesticides and health risks. Muhammad submitted to KUST, Pakistan under the title “Screening J. Obstet. Gynecol. Neonatal. Nurs. 39, 103-110. of Neem seeds and Turmeric rhizome extracts for biopesticidal activi- Girish, K., Shankara, Bhat, S., 2008: Neem a green treasure. Electronic ties against aphids in okra”. J. Biol. 4, 201-111. Hafeez, F,. Zia, K., 2009: Relative resistance of different maize varieties Authors contributions: against insect pest complex harboring crop ecology. J. Agric. Soc. Sci. UM and TNK: Conducted experiments 5, 52-54. HR, MKD and WM: Data analysis; initial drafting of publication Hamill, A.S., Holt, J.S., Mallory-Smith, C.A., 2004: Contributions of AA: Designed experiments; overall supervision of experiments; final weed science to weed control and management. Weed Technol. 18, 1563- drafting and correction 1565. Hashmat, I., Azad, H., Ahmed, A., 2012: Neem a nature’s drugstore: an overview. Int. Res. J. Bio. Sci. 1, 76-9. References Hossain, M.D., Yasmin, S., Latif, M.A., Akhter, N., 2013: Effect of Neem Abida, Y., Tabassum, F., Zaman, S., Chhabi, S.B., Islam, N., 2009: and other Plant Extracts on Yellow Mite of Jute. Int. J. Bio-Reso. Stress Biological screening of Curcuma longa for insecticidal and repellent Manage. 4, 412-417. potentials against Tribolium castaneum adults. University Journal of Iqbal, J., Ali, H., Hassan, M.W., Jamil, M., 2015: Evaluation of indigenous Zoology, Rajshahi University 28, 69-71. plant extracts against sucking insect pests of okra crop. Pak. Entomol. Adesina, J.M., Afolabi, L.A., 2014: Comparative bio-efficacy of aqueous 37, 39-44. extracts of Loncarpous cyanescens and Trema orientalis against flea Iqbal, J., Qayyum, A., Mustafa, S.Z., 2010: Repellent effect of ethanol ex- beetle (Podagrica spp.) Infestation and Yield of Okra. Int. J. Horticul- tracts of plant materials on Tribolium castaneum (Herbst) (Coleoptera). ture 4. Pak. J. Zoo. 42, 81-6. Ahmed, M.M., 2000: Studies on the control of insect pests in vegetables James, A.O., Akinrinade, A., Olufisayo, I., 2014: Evaluation of botanical (okra, tomato and onion) in Sudan with special reference to neem prepa- insecticides against flea beetles Podagrica sjostedti and Podagrica uni- rations. Doctoral Dissertation, University of Göttingen, Germany. forma of okra. Int. J. Adv. Res. 2, 236-244 . Ajaiyeoba, E.O., Sama, W., Essien, E.E., Olayemi, J.O., Ekundayo, O., Jbilou, R., Ennabili, A., Sayah, F., 2006: Insecticidal activity of four me- Walker, T.M., Setzer, W.N., 2008: Larvicidal activity of turmerone- dicinal plant extracts against Tribolium castaneum (Herbst) (Coleop- rich essential oils of Curcuma longa. Leaf and rhizome from Nigeria on tera: Tenebrionidae). Afr. J. Biotechnol. 16, 5-10. Effects of Neem seed and Turmeric rhizome extracts on aphids control in okra 201

Kashif, S., Yaseen, M., Arshad, M.U., Ayub, M., 2008: Response of okra associated natural enemies in spring potato crop, Peshawar, Pakistan. to soil given encapsulated calcium carbide. Pak. J. Bot. 40, 175. Sarhad J. Agric. 25, 451-456. Khan, A.M., Khan, A.A., Afzal, M., Iqbal, M.S., 2012: Wheat crop yield Sankari, S.A., Narayanasamy, P., 2007: Bio-efficacy of flyash-based losses caused by the aphids infestation. J. Biofertil. Biopestic. 2, 122 herbal pesticides against pests of rice and vegetables. Current Science Kiely, T., Donaldson, D., Grube, A., 2004: Pesticides industry sales Bangalore 92, 811. and usage: 2000 and 2001 market estimates. Washington, DC: US Satti, A.A., Nasr, O.E., 2008: The First African congress on pesticides Environmental Protection Agency. 2004 May, 114. and toxicology sciences, Gezira University, Wad Medani/Sudan, 8-11 Li, S., Yuan, W., Deng, G., Wang, P., Yang, P., Aggarwal, B., 2011: Savary, S., Teng, P.S., Willocquet, L., Nutter, Jr, F.W., 2006: Quanti- Chemical composition and product quality control of turmeric. Faculty fication and modeling of crop losses: a review of purposes. Ann. Rev. Publications Paper 1. http://scholarworks.sfasu.edu/agriculture_faculty- Phytopathol. 44, 89-112. pubs/1 Schmutterer, H., 1990: Future tasks of neem research in relation to Lokanadhan, S., Muthukrishnan, P., Jeyaraman, S., 2012: Neem pro- agricultural needs worldwide. ARS-US Department of Agriculture, ducts and their agricultural applications. J. Biopestic. 5, 72-76. Agricultural Research Service (USA). Magné, C., Saladin, G., Clément, C., 2006: Transient effect of the her- Shabozoi, N.U., Abro, G.H., Syed, T.S., Awan, M.S., 2011: Economic ap- bicide flazasulfuron on carbohydrate physiology in Vitis vinifera. praisal of pest management options in Okra. Pak. J. Zoo. 43, 869-878. Chemosphere 62, 650-700. Shah, J.A., Inayatullah, M., Sohail, K., Shah, S.F., Shah, S., Iqbal, T., Matter, M.M., Salem, S.A., Abou-Ela, R.G., El-Kholy, M.Y., 2008: Usman, M., 2013: Efficacy of botanical extracts and a chemical pesticide Toxicity and repellency of Trigonella foenum and Curcuma longa ex- against tomato fruit worm, (Helicoverpa Armigera). Sarhad J. Agric. 29, tracts to Sitophilus oryzae and Rhizopertha dominica (Coleoptera). Egy. 93-6. J. Biol. Pest Cont. 18, 149-154. Siddiqi, A.R., Rafi, A., Naz, F., Masih, R., Ahmad, I., Jilani, G., 2011: Mudathir, M., Basedow, T.H., 2004: Field experiments on the effects of Effects of Curcuma longa extracts on mortality and fecundity of neem products on pests and yields of okra, tomato, and onion in the Bactrocera zonata (Diptera: Tephritidae). Ciência e Agrotecnologia. 35, Sudan. In: Mitteilungen der Deutschen Gesellschaft für allgemeine und 1110-1114. angewandte Entomologie 14, 407-410. Sohail, K., Jan, S., Shah, S.F., Ali, H., Farooq, M., Ashfaq, S., 2015: Okwute, S.K., 2012: Plants as potential sources of pesticidal agents: a re- Evaluation of botanical and chemical insecticides against the insect pest view. In Tech Open Access Publisher. of okra. J. Entomol. Zoo. Stud. 3, 20-24 Ostermann, H., 1992: Zur Wirkung und Anwendung einfacher Niempro- Su, M., 1999: Activity and biological effects of neem products against arthro- dukte gegen Schädlinge in kleinbäuerlichen Tomaten-, Vignabohnen- pods of medical and veterinary importance. J. Am. Mosq. Cont. Assoc. und Amaranthkulturen im Niger. Wiss. Fachverl. Ph.D thesis, 181. 15, 133-152. Germany. Walley, F., Taylor, A., Lupwayi, N., 2006: Herbicide effects on pulse crop Oyelade, O.J., Ade-Omowaye, B.I., Adeomi, V.F., 2003: Influence of va- nodulation and nitrogen fixation. Farm Technology Proceedings, 121- riety on protein, fat contents and some physical characteristics of okra 123. seeds. J. Food Eng. 57, 111-114. Pimentel, D., 2007: Area-wide pest management: environmental, eco- Address of the corresponding author: nomic and food issues. In: Area-wide control of insect pests Springer Dr. Azizullah, Assistant Professor, Department of Botany, Kohat University of Netherlands, 35-47. Science and Technology, 26000 Kohat, Pakistan Rajaram, V., Mathirajan, V.G., Krishnasamy, S., 2006: IPM in cotton E-mail: [email protected] under dry farming condition. Int. J. Agric. Sci. 2, 557-558. Roy, G.C., Chakraborty, K., Nandy, P., Moitra, M.N., 2015: Pros and © The Author(s) 2018. cons of curcumin as bioactive phyto-compound for effective manage- This is an Open Access article distributed under the terms ment of insect pests. Am. Sci. Res. J. Eng. Technol. Sci. 7, 31-43. of the Creative Commons Attribution Share-Alike License (http://creative- Saljoqi, A., 2009: Population dynamics of Myzus persicae (Sulzer) and its commons.org/licenses/by-sa/4.0/).